Dinoflagellates are a diverse group of microplankton that include free-living, symbiotic, and parasitic species. Amoebophrya, a basal lineage of parasitic dinoflagellates, infects a variety of marine microorganisms, including harmful-bloom-forming algae. Although there are currently three published Amoebophrya genomes, this genus has considerable genomic diversity. We add to the growing genomic data for Amoebophrya with an annotated genome assembly for Amoebophrya sp. ex Karlodinium veneficum. This species appears to translate all three canonical stop codons contextually. Stop codons are present in the open reading frames of about half of the predicted gene models, including genes essential for cellular function. The in-frame stop codons are likely translated by suppressor tRNAs that were identified in the assembly. We also assembled the mitochondrial genome, which has remained elusive in the previous Amoebophrya genome assemblies. The mitochondrial genome assembly consists of many fragments with high sequence identity in the genes but low sequence identity in intergenic regions. Nuclear and mitochondrially-encoded proteins indicate that Amoebophrya sp. ex K. veneficum does not have a bipartite electron transport chain, unlike previously analyzed Amoebophrya species. This study highlights the importance of analyzing multiple genomes from highly diverse genera such as Amoebophrya.